The transition of growing plants from vegetative growth to flowering is the major developmental switch in the plant life cycle. The timing of flower initiation is critical for the reproductive success of wild plants, and most plant species have evolved systems to precisely regulate flowering time. These systems monitor both environmental cues and the developmental state of the plant to control flowering.
Two commonly monitored environmental cues are photoperiod and temperature. In the photoperiod-responsive plants so examined, daylength is perceived in leaves and flowering signals appear to be translocated from leaves to meristems (Zeevaart, Light and the Flowering Process, Process, eds., D. Vince-Prue, B. Thomas and K. E. Cockshull, 137–142, Academic Press, Orlando, 1984.). Exposure to cold temperatures promotes flowering by a process known as vernalization. Vernalization affects meristems directly, perhaps by causing them to become competent to perceive flowering signals (Lang, Encyclopedia of Plant Physiology, ed., W. Ruhland, 15 (Part 1), 1371–1536, Springer-Verlag, Berlin, 1965). Other environmental cues that can affect flowering include light quality and nutritional status.
The developmental state of the plant can also influence flowering time. Most species go through a juvenile phase during which flowering is suppressed, and eventually undergo a transition to an adult phase in which the plant is competent to flower (Poethig, Science, 250, 923–930, 1990). This “phase change” permits the plant to reach a proper size for productive flowering.
In the flowering literature, the developmental flowering pathways are often referred to as autonomous to indicate that they do not involve the sensing of photoperiod. However, it is unlikely that autonomous and photoperiod pathways are entirely distinct. For example, day-neutral species of tobacco flower after producing a specific number of nodes and thus could be classified as flowering entirely through an autonomous pathway, but grafting studies indicate that day-neutral and photoperiod-responsive tobacco species respond to similar translocatable flowering signals (Lang et al., Proc. Natl. Acad. Sci., USA, 74, 2412–2416, 1977; McDaniel et al., Plant J., 9, 55–61, 1996). Thus aspects of the underlying biochemistry of these pathways appear to be conserved.
Genetic analyses in several species has identified genes that affect the timing of flowering. The most extensive genetic analysis of flowering-time genes has been performed in Arabidopsis thaliana. In Arabidopsis, flowering-time genes have been identified by two approaches. One approach has been to induce mutations that affect flowering time in early-flowering varieties. Such mutations can cause either late-flowering or even earlier flowering. Late-flowering mutations identify genes whose wild-type role is to promote flowering and early-flowering mutations identify inhibitory ones. Studies in Arabidopsis have identified over 20 loci for which mutations specifically affect flowering time and several other loci that affect flowering time as well as other aspects of development (e.g., det2, cop1, gal and phyB) (Koornneef et al., Ann. Rev. Plant Physiol., Plant Mol. Biol., 49, 345–370, 1998; Weigel, Ann. Rev. Genetics, 29, 19–39, 1995).
Another approach to identify flowering-time genes is to determine the genetic basis of naturally occurring variation in flowering time. Although the varieties of Arabidopsis most commonly used in the laboratory are early-flowering (summer annuals), most varieties are late-flowering (winter annuals). Late-flowering varieties differ from early-flowering ones in that the late-flowering varieties contain dominant alelles at two loci, FRIGIDA (FRI) and FLOWERING LOCUS C (FLC) that suppress flowering (Sanda et al., Plant Physiol., 111, 641–645, 1996; Lee et al., Plant Journal, 6, 903–909, 1994; Clarke et al., Mol. Gen. Genet., 242, 81–89, 1994; Koornneef et al., Plant Journal, 6, 911–919, 1994).
Physiological analyses of flowering-time mutants and naturally occurring variation in flowering time indicate that flowering is controlled by multiple pathways in Arabidopsis (Koornneef et al., Ann. Rev. Plant Physiol., Plant Mol. Biol., 49, 345–370, 1998). One group of late-flowering mutants (fca, fpa, fve, fy, ld) and plants containing the late-flowering FLC and FRI alleles are delayed in flowering in inductive (long-day) conditions and are even more severely delayed in short days. Vernalization of these late-flowering lines can suppress the late-flowering phenotype. Another group of late-flowering mutants (co, fd, fe, fha, ft, fwa, gi) exhibit a slight or no difference in flowering time when grown in short days compared to long days. Furthermore, this group shows little or no response to vernalization. Double mutants within a group do not flower significantly later than either single-mutant parent, whereas double mutants containing a mutation in each group flower later than the single-mutant parents (Koornneef et al., Genetics, 148, 885–92, 1998). Thus, there appears to be parallel flowering pathways that mediate the flowering response to environmental and developmental cues. A photoperiod pathway promotes flowering in long days. A pathway referred to in the literature as autonomous appears to control the age, or more specifically the developmental stage, at which plants are competent to flower. Recent support of the developmental role of this pathway is the demonstration that autonomous pathway mutants exhibit changes such as alterations of trichome patterns that indicate such mutant plants are delayed in the juvenile to adult transition (Telfer et al., Development, 124, 645–654, 1997).
Blocks to the autonomous pathway due to mutant fca, fpa, fve, fy, and ld alleles or to the presence of dominant late-flowering FLC and FRI alleles can be bypassed by vernalization (Koornneef et al., Ann. Rev. Plant Physiol., Plant Mol. Biol., 49, 345–370, 1998). Thus FLC and FRI can be regarded as genes that create a requirement for vernalization. Other species, particularly Brassicas, appear to have the same “circuitry” as Arabidopsis. This similarity has been most thoroughly analyzed for the relationship between dominant suppressors of flowering and vernalization in Brassicas. The major difference between annual and biennial cultivars of oilseed Brassica napus and B. rapa is conferred by genes controlling vernalization-responsive flowering time (Osborn et al., Genetics Society of America, 146, 1123–1129, 1997). By comparing quantitative trait loci (QTLs) in segregating populations of annual X biennial varieties of B. rapa and B. napus, it was shown that the 2 major QTLs that confer vernalization-responsive late flowering in B. napus and B. rapa are likely to be the same (Osborn et al., Genetics Society of America, 146, 1123–1129, 1997). In B. rapa the two flowering-time QTLs were separated in recombinant inbred populations and the QTL with the greatest effect on flowering time was VFR2 (vernalization-responsive flowering time in rapa 2). Furthermore, VFR2 appears to correspond to FLC from Arabidopsis: VFR2 was mapped at high resolution using hybridization probes that permit a comparison of Arabidopsis and Brassicas after introgression of the late allele into the early-flowering annual variety, and only a probe corresponding to FLC detected no recombination events with VFR2 (<0.44 cm) indicating that VFR2 is an FLC homolog.
The timing of flowering is of great importance in both agricultural and horticultural crops. In horticultural crops the product is often the flowers. In food, feed crops, or fiber crops, such as the cereals rice, wheat, maize, barley, oats, soybeans, canola, cotton, sunflower, tomato, and broccoli, the product is often the flower or the result of flowering—fruits, seeds, or seedpods. Identifying new genes that are involved in flowering-time control will lead to new strategies to optimize flower, fruit, and seed production by genetic manipulations. For example, in certain crops accelerating the onset of flowering would permit the crops to be grown in a region where the growing season is otherwise too short, or permit multiple crops in a region where only one crop is currently possible.
There are also crops in which the non-flowering parts of the plant are the useful parts. In such crops preventing or substantially delaying flowering will increase the yield of these useful parts. Examples of plants in which delaying or preventing flowering would be desirable include forage crops such as alfalfa and clover, and vegetables such as cabbage and related Brassicas, spinach and lettuce. In crops in which underground parts are used, such as sugar beet or potato, delaying or preventing flowering should increase yield. Also, in sugar beet, prevention of flowering will permit more energy to be devoted to sugar production. Likewise the yield of wood and biomass crops will be increased by delaying flowering. Identifying new genes that are involved in flowering time control will provide new tools to delay flowering in the above plants.